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Pollak, S.

Publications and source records attributed to Pollak, S..

4 recordsLinked to original sources

Fundamental metabolic strategies of heterotrophic bacteria

Through their metabolism, heterotrophic microbes drive carbon cycling in many environments (1). These microbes consume (and produce) hundreds to thousands of different metabolic substrates, begging the question of what level of description is required to understand the metabolic processes structuring their communities: do we need to account for the detailed metabolic capabilities of each organism, or can these capabilities be understood in terms of a few well-conserved carbon utilization strategies that could be more easily interpreted and more robustly predicted? Based on the high-throughput phenotyping of a diverse collection of marine bacteria, we showed that the fundamental metabolic strategy of heterotrophic microbes can be understood in terms of a single axis of variation, representing their preference for either glycolytic (sugars) or gluconeogenic (amino and organic acids) carbon sources. Moreover, an organisms position on this axis is imprinted in its genome, allowing us to successfully predict metabolic strategy across the bacterial tree of life. Our analysis also unveils a novel and general association between metabolic strategy and genomic GC content, which we hypothesize results from the difference in C:N supply associated with typical sugar and acid substrates. Thus, our work reveals a fundamental constraint on microbial evolution that structures bacterial genomes and communities and can be leveraged to understand diversity in functional terms, beyond catalogs of genes and taxa.

microbiology↗

Ecological stochasticity and phage induction diversify bacterioplankton communities at the microscale

In many natural environments, microorganisms self-assemble around heterogeneously distributed resource patches. The growth and collapse of populations on resource patches can unfold within spatial ranges of a few hundred micrometers or less, making such microscale ecosystems hotspots of biological interactions and nutrient fluxes. Despite the potential importance of patch-level dynamics for the large-scale evolution and function of microbial communities, we have not yet been able to delineate the ecological processes that control natural populations at the microscale. Here, we addressed this challenge in the context of microbially-mediated degradation of particulate organic matter by characterizing the natural marine communities that assembled on over one thousand individual microscale chitin particles. Through shotgun metagenomics, we found significant variation in microscale community composition despite the similarity in initial species pools across replicates. Strikingly, a subset of particles was highly populated by rare chitin-degrading strains; we hypothesized that their conditional success reflected the impact of stochastic colonization and growth on community assembly. In contrast to the conserved functional structures that emerge in ecosystems at larger scales, this taxonomic variability translated to a wide range of predicted chitinolytic abilities and growth returns at the level of individual particles. We found that predation by temperate bacteriophages, especially of degrader strains, was a significant contributor to the variability in the bacterial compositions and yields observed across communities. Our study suggests that initial stochasticity in assembly states at the microscale, amplified through biotic interactions, may have significant consequences for the diversity and functionality of microbial communities at larger scales. Significance StatementThe biogeochemical consequences of the degradation of particulate organic matter by microorganisms represent the cumulative effect of microbial activity on individual microscale resource patches. The ecological processes controlling community dynamics in these highly localized microenvironments remain poorly understood. Here, we find that complex marine communities growing on microscale resource particles diverge both taxonomically and functionally despite assembling under identical abiotic conditions from a common species pool. We show that this variability stems from bacteriophage predation and history-dependent factors in community assembly, which create stochastic dynamics that are spatially structured at the microscale. This microscale stochasticity may have significant consequences for the coexistence, evolution, and function of diverse bacterial and viral populations in the global ocean.

microbiology↗

Hierarchical control of microbial community assembly

Metabolic processes that fuel the growth of heterotrophic microbial communities are initiated by specialized biopolymer degraders that decompose complex forms of organic matter. It is unclear, however, to what extent degraders control the downstream assembly of the community that follows polymer breakdown. Investigating a model marine microbial community that degrades chitin, we show that chitinases secreted by different degraders produce oligomers of specific chain lengths that not only select for specialized consumers but also influence the metabolites secreted by these consumers into a shared resource pool. Each species participating in the breakdown cascade exhibits unique hierarchical preferences for substrates, which underlies the sequential colonization of metabolically distinct groups as resource availability changes over time. By identifying the metabolic underpinnings of microbial community assembly, we reveal a hierarchical crossfeeding structure that allows biopolymer degraders to shape the dynamics of community assembly. One sentence summarySpecialized biopolymer degraders direct the trajectory of microbial community assembly through interconnected modes of nutrient crossfeeding.

microbiology↗

Public good exploitation in natural bacterioplankton communities

Microorganisms such as bacteria often interact with their environment through extracellular molecules that increase access to limiting resources. These secretions can act as public goods, creating incentives for exploiters, a.k.a cheaters, to invade and steal public goods away from producers. This phenomenon has been studied extensively in microbiology due to its implications for the evolution of cooperation, but little is known about the occurrence and impact of public good exploiters in the environment. Here, we develop a new genomic approach to systematically identify bacteria that can exploit public goods produced during the degradation of polysaccharides. Focusing on chitin - the second most abundant biopolymer on the planet, we show that public good exploiters are active in natural marine microbial communities that assemble on chitin particles, invading during early stages of colonization and potentially hindering degradation. Unlike in classical studies of social evolution, exploiters and polysaccharide degraders are not isogenic and instead belong to distant lineages, facilitating their coexistence. Our approach opens novel avenues to use the wealth of genomic data available to infer ecological roles and interactions among microbes.

microbiology↗